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Craniometric Analysis of the Hindbrain and Craniocervical Junction Of RESEARCH ARTICLE Craniometric Analysis of the Hindbrain and Craniocervical Junction of Chihuahua, Affenpinscher and Cavalier King Charles Spaniel Dogs With and Without Syringomyelia Secondary to Chiari-Like Malformation Susan P. Knowler1*, Anna-Mariam Kiviranta2, Angus K. McFadyen3, Tarja S. Jokinen2, a1111111111 Roberto M. La Ragione1, Clare Rusbridge1,4 a1111111111 a1111111111 1 School of Veterinary Medicine, Faculty of Health & Medical Sciences, University of Surrey, Guildford, Surrey, United Kingdom, 2 Department of Equine and Small Animal Medicine, 00014 University of Helsinki, a1111111111 Finland, 3 akm-stats, Glasgow, Scotland, United Kingdom, 4 Fitzpatrick Referrals, Godalming, Surrey, a1111111111 United Kingdom * [email protected] OPEN ACCESS Abstract Citation: Knowler SP, Kiviranta A-M, McFadyen AK, Jokinen TS, La Ragione RM, Rusbridge C (2017) Objectives Craniometric Analysis of the Hindbrain and To characterize and compare the phenotypic variables of the hindbrain and craniocervical Craniocervical Junction of Chihuahua, Affenpinscher and Cavalier King Charles Spaniel junction associated with syringomyelia (SM) in the Chihuahua, Affenpinscher and Cavalier Dogs With and Without Syringomyelia Secondary King Charles Spaniel (CKCS). to Chiari-Like Malformation. PLoS ONE 12(1): e0169898. doi:10.1371/journal.pone.0169898 Method Editor: Carlos E. AmbroÂsio, Faculty of Animal Analysis of 273 T1-weighted mid-sagittal DICOM sequences of the hindbrain and craniocer- Sciences and Food Engineering, University of São Paulo, BRAZIL vical junction from 99 Chihuahuas, 42 Affenpinschers and 132 CKCSs. The study compared 22 morphometric features (11 lines, eight angles and three ratios) of dogs with and without Received: August 19, 2016 SM using refined techniques based on previous studies of the Griffon Bruxellois (GB) using Accepted: December 23, 2016 Discriminant Function Analysis and ANOVA with post-hoc corrections. Published: January 25, 2017 Copyright: © 2017 Knowler et al. This is an open Results access article distributed under the terms of the The analysis identified 14/22 significant traits for SM in the three dog breeds, five of which Creative Commons Attribution License, which permits unrestricted use, distribution, and were identical to those reported for the GB and suggest inclusion of a common aetiology. reproduction in any medium, provided the original One ratio, caudal fossa height to the length of the skull base extended to an imaginary point author and source are credited. of alignment between the atlas and supraoccipital bones, was common to all three breeds (p Data Availability Statement: All relevant data are values 0.029 to <0.001). Associated with SM were a reduced occipital crest and two acute within the paper and its Supporting Information changes in angulation i) `sphenoid flexure' at the spheno-occipital synchondrosis ii) `cervical files. flexure' at the foramen magnum allied with medulla oblongata elevation. Comparing dogs Funding: Cavalier Matters Charity Reg No 1141674 with and without SM, each breed had a unique trait: Chihuahua had a smaller angle between http://www.cavaliermatters.org/ funded SPK's the dens, atlas and basioccipital bone (p value < 0.001); Affenpinschers had a smaller dis- doctoral research. Dogs Trust Charity Reg. No. 227523 & SC037843, https://www.dogstrust.org. tance from atlas to dens (p value 0.009); CKCS had a shorter distance between the spheno- uk/ contributed towards the cost of leasing the occipital synchondrosis and atlas (p value 0.007). PLOS ONE | DOI:10.1371/journal.pone.0169898 January 25, 2017 1 / 18 Craniometric Analysis of Three Breeds With and Without Syringomyelia DICOM viewing software package MIMICS 14.12 Conclusion Materialise (Technologielaan 15 3001 Leuven Belgium). The Finnish Veterinary Foundation The selected morphometries successfully characterised conformational changes in the funded the costs of the imaging at the Veterinary brain and craniocervical junction that might form the basis of a diagnostic tool for all breeds. Teaching Hospital of University of Helsinki. Henny The severity of SM involved a spectrum of abnormalities, incurred by changes in both angu- van/der Berg donated the photo morphing software lation and size that could alter neural parenchyma compliance and/or impede cerebrospinal AbrosoftFantaMorph. Rupert's Fund (www. rupertsfund.com) and For the Love of Ollie (www. fluid channels. fortheloveofollie.com) provided financial support for health screening. AKM is an independent statistical consultant operating professionally as a sole trader under the company name of akm-stats and did not receive any salary or other remittance Introduction for his contribution in this investigation. The Syringomyelia (SM) secondary to Chiari-like malformation (CM) is diagnosed increasingly in funders had no role in study design, data collection and analysis, decision to publish, or preparation of toy breed dogs [1]. Since both of these conditions can be accompanied by pain and /or neuro- the manuscript. logical deficits [2±4], there are associated welfare concerns and a desire to reduce the disease prevalence in predisposed breeds [5]. CM, sometimes referred to as caudal occipital malforma- Competing Interests: SPK is a post graduate research student at the University of Surrey where tion syndrome (COMS), is a complex developmental abnormality of the skull and craniocervi- CR and RMLaR are employed. CR is also are cal junction. It is usually defined as a mismatch between size of the brain and the caudal fossa employed by Fitzpatrick Referrals Ltd, Surrey. A- leading to cerebellar and brainstem herniation [6±8]. Recently other research studies have MK and TJ are employed by the University of reported that CM is characterized by the shortening of the skull base, reduced caudal cranial Helsinki. AKM is an independent statistical fossa volume and increased proximity of the cranial cervical vertebrae to the skull [9, 10]. The consultant operating professionally as a sole trader under the company name of akmstats and did not mismatch of the skull and brain, like its human equivalent Chiari type I and O malformation receive any salary or other remittance for his (CM1 and CM0) [11], disrupts the cerebrospinal fluid (CSF) flow dynamics which may be pro- contribution in this investigation. Fitzpatrick gressive over time [12±14] with resultant CSF-like fluid cavitation in the spinal cord known as Referrals Ltd and the Universites of Surrey and SM [15, 16]. Finland did not play a role in the study design, data The Cavalier King Charles Spaniel (CKCS) has a high prevalence for CM/SM which has collection and analysis, decision to publish, or been well documented over the last decade and contributed to a considerable knowledge base preparation of the manuscript and only provided financial support in the form of authors' salaries for these conditions [17]. CM is ubiquitous in the CKCS breed and it is likely that additional and/or research materials. None of the authors risk factors account for a predisposition to SM [18]. However, in a recent study investigating have personal or financial relationships with other the prevalence of CM in clinically unaffected dogs, it was concluded that the high prevalence people or organizations that might inappropriately of cerebellar indentation and impaction in toy breeds may be ªnormalº anatomical variations influence or bias the content of the paper. There are [19]. The inheritance of CM/SM is complex [20, 21] and it has been shown to have a multifac- no patents, products in development, or marketed products to declare. This does not alter the torial relationship between CM and SM in the CKCS [22, 23] and the Griffon Bruxellois (GB) authors' adherence to PLOS ONE policies on [9, 24]. sharing data and materials. Two particular risk factors associated with CM/SM are miniaturization and brachycephaly [25±27]. The Chihuahua is the smallest known dog breed for which SM has been reported. Both British and American breed standards state that a Chihuahua must not weigh more than 2.7 kg (6 lb). An investigation of this miniature breed may therefore elucidate the pathogenesis of CM/SM. The Affenpinscher is a brachycephalic dog, often referred to as the ªmonkey dogº. It is quite similar in appearance to the GB but typically larger and with a less stocky build. Although the Affenpinscher wirehaired head has rostrocaudal shortening similar to the GB, its muzzle is not as flattened [28] and provides an interesting brachycephalic variation for CM/ SM investigation. Study objectives This study compares Magnetic Resonance images (MRI) taken in the mid-sagittal plane obtained from three breeds, the CKCS, Affenpinscher and Chihuahua, using refined morpho- metric techniques that were originally developed to investigate the genetic basis of CM in the Griffon Bruxellois (GB). The study aims were: PLOS ONE | DOI:10.1371/journal.pone.0169898 January 25, 2017 2 / 18 Craniometric Analysis of Three Breeds With and Without Syringomyelia 1. Characterize the phenotypic variables of the caudal fossa and craniocervical junction associ- ated with SM (i.e. characterize the phenotypic variables of canine CM). 2. Elucidate any conformation similarities between the breeds that might suggest a common aetiology and assist in diagnosis. 3. Identify any protective conformation traits that might contribute to generating estimated breeding values in order to reduce the risk of SM through selective breeding. Ethics statement This retrospective study analysed Digital
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